Nematophagous fungus Arthrobotrys oligospora mimics olfactory cues of sex and food to lure its nematode prey

Abstract

To study the molecular basis for predator-prey coevolution, we investigated how <i>Caenorhabditis elegans</i> responds to the predatory fungus <i>Arthrobotrys oligospora</i>. <i>C. elegans</i> and other nematodes were attracted to volatile compounds produced by <i>A. oligospora</i>. Gas-chromatographic mass-spectral analyses of <i>A. oligospora</i>-derived volatile metabolites identified several odors mimicking food cues attractive to nematodes. One compound, methyl 3-methyl-2-butenoate (MMB) additionally triggered strong sex- and stage-specific attraction in several <i>Caenorhabditis</i> species. Furthermore, when MMB is present, it interferes with nematode mating, suggesting that MMB might mimic sex pheromone in <i>Caenorhabditis</i> species. Forward genetic screening suggests that multiple receptors are involved in sensing MMB. Response to fungal odors involves the olfactory neuron AWCs. Single-cell RNA-seq revealed the GPCRs expressed in AWC. We propose that <i>A. oligospora</i> likely evolved the means to use olfactory mimicry to attract its nematode prey through the olfactory neurons in <i>C. elegans</i> and related species.